Acta Palaeontol. Pol. 61 (2): 281–292, 2016 http://dx.doi.org/10.4202/app.00132.2014
Ontogenetic changes in the craniomandibular skeleton
of the abelisaurid dinosaur
Majungasaurus crenatissimus
from the Late Cretaceous of Madagascar
NIRINA O. RATSIMBAHOLISON, RYAN N. FELICE, and PATRICK M. O’CONNOR
Ratsimbaholison, N.O., Felice, R.N., and O’Connor, P.M. 2016. Ontogenetic changes in the craniomandibular skeleton of the abelisaurid dinosaur Majungasauruscrenatissimus from the Late Cretaceous of Madagascar. Acta Palaeontologica Polonica 61 (2): 281–292.
Abelisaurid theropods were one of the most diverse groups of predatory dinosaurs in Gondwana during the Cretaceous. The group is characterized by a tall, wide skull and robust cervical region. This morphology is thought to have facilitated specialized feeding behaviors such as prolonged contact with prey. The Late Cretaceous abelisaurid Majungasaurus crenatissimus typifies this abelisaurid cranial morphotype. Recent fossil discoveries of this species include a partial growth series that allows for the first time an investigation of ontogenetic variation in cranial morphology in a repre-sentative abelisaurid. Herein we examine growth trajectories in the shape of individual cranial bones and articulated skulls of Majungasaurus using geometric morphometrics. Several major changes in skull shape were observed through ontogeny, including an increase in the height of the jugal, postorbital, and quadratojugal, an increase in the extent of the contacts between bones, and a decrease in the circumference of the orbit. The skull transitions from relatively short in the smallest individual to tall and robust in large adults, as is seen in other theropods. Such morphological change during ontogeny would likely have resulted in different biomechanical properties and feeding behaviors between small and large individuals. These findings provide a post-hatching developmental framework for understanding the evolution of the distinctive tall skull morphology seen in abelisaurids and other large-sized theropod dinosaurs.
Key words: Dinosauria, Abelisauridae, geometric morphometrics, ontogeny, skull, Cretaceous, Gondwana.
Nirina O. Ratsimbaholison [ratsimbano@gmail.com], Department of Paleontology and Biological Anthropology, Uni-versity of Antananarivo, BP 906, Antananarivo 101, Madagascar; Ohio Center for Ecology and Evolutionary Studies, 228 Irvine Hall, Athens, Ohio 45701 USA.
Ryan N. Felice [ryanfelice@gmail.com], Ohio Center for Ecology and Evolutionary Studies, 228 Irvine Hall, Athens, Ohio 45701 USA; Department of Biological Sciences, Ohio University, 228 Irvine Hall, Athens, Ohio 45701, USA; cur-rent address: Department of Genetics, Evolution and Environment, University College London, London, UK.
Patrick M. O’Connor [oconnorp@ohio.edu] (corresponding author), Ohio Center for Ecology and Evolutionary Stud-ies, 228 Irvine Hall, Athens, Ohio 45701 USA; Department of Biomedical Sciences, Ohio University Heritage College of Osteopathic Medicine, 228 Irvine Hall, Athens, Ohio 45701, USA.
Received 14 October 2014, accepted 20 January 2016, available online 17 February 2016.
Copyright © 2016 N.O. Ratsimbaholison et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (for details please see http://creativecommons.org/licenses/by/4.0/), which permits unre-stricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Introduction
It is well appreciated that Tyrannosauridae occupied the large-predator niche in the Northern Hemisphere during the Late Cretaceous. By contrast, abelisaurids were among the most diverse non-avian theropod dinosaurs on Gondwanan landmasses during this same interval. Abelisaurids are con-sidered members of Ceratosauria (Carrano and Sampson 2008), a diverse lineage of Jurassic through Cretaceous theropod dinosaurs that exhibit a vast array of body sizes and morphologies (Gilmore 1920; Madsen and Welles 2000;
2008), India (Indosaurus matleyi, Huene and Matley 1933; Novas et al. 2004; Rajasaurus narmadensis, Wilson et al. 2003), Madagascar (Majungasauruscrenatissimus, Depéret 1896a, b; Sampson et al. 1998; Sampson and Witmer 2007; Dahalokely tokana, Farke and Sertich 2013), continental Africa (Rugopsprimus, Sereno et al. 2004; Kryptopspalaios, Sereno and Brusatte 2008) and adjacent areas (e.g., southern Europe; Genusaurus sisteronis, Accarie et al. 1995). These discoveries have provided a glimpse of regional diversity and variability within the clade (Carrano and Sampson 2008; Novas et al. 2013; Méndez 2014).
Among the best known of the abelisaurids is Majunga-saurus crenatissimus from the Upper Cretaceous Maevarano Formation exposed in northwestern Madagascar (Sampson and Krause 2007). The skull of this taxon was thoroughly described (Sampson and Witmer 2007) on the basis of well-preserved materials; this taxon typifies the charac-teristic tall, rostrocaudally short and dorsoventrally tall skull of Abelisauridae. Several additional skulls and partial skeletons have since been recovered that represent multi-ple, size-diverse specimens (O’Connor et al. 2011; Burch and Carrano 2012). As such, Majungasaurus (Fig. 1) has emerged as one of the best-documented species of non-avian theropod dinosaurs from Gondwana, allowing for the first time the formulation of questions related to characterizing intraspecific and ontogenetic variation in Abelisauridae.
Geometric morphometric approaches are commonly used to quantify and visualize interspecific or intraspecific shape variation across a number of specimens or species (e.g., Rohlf and Marcus 1993; Adams et al. 2004, 2013; Zelditch et al. 2004). These approaches have been used to examine topics ranging from assessing basic shape variation (Breuker et al. 2006; Piras et al. 2011; Openshaw and Keogh 2014), justify-ing species assignments (Baltanás and Danielopol 2011; De Meulemeester et al. 2012), developing biomechanical models (Sakamoto 2010), and testing macroevolutionary hypotheses (e.g., resource partitioning; Kassam et al. 2003).
Morphometric studies have also been used in many pa-leontological applications, ranging from studies aimed at understanding the locomotor potential in now-extinct clades (Bonnan 2007) to characterizing tempo and mode of cranial evolution (Meloro and Jones 2012), with many recent exam-ples from invertebrate (e.g., Baltanás and Danielopol 2011; Webster and Zelditch 2011) and vertebrate (e.g., Chapman 1990; Stayton and Ruta 2006; Schott et al. 2011; Martin-Serra et al. 2014) groups. Geometric morphometric stud-ies have less frequently focused on dinosaurs, although a recent interest in applying these approaches to the group has resulted in a number of studies (e.g., Young and Larvan 2010; Campione and Evans 2011; Foth and Rauhut 2013a, b; Hedrick and Dodson 2013; Maoirino et al. 2013). Several efforts have examined the skull of non-avian theropod di-nosaurs, quantifying aspects of craniofacial variability such as cranial diversity and shape disparity, modeling function among different cranial morphs, and hypothesizing puta-tive evolutionary processes producing shape variability in the clade (Young et al. 2010; Zanno and Makovicky 2011; Bhullar et al. 2012; Brusatte et al. 2012; Foth 2013; Foth and Rauhut 2013a). For example, Carpenter (1990) found (qual-itatively) that individual variation for Tyrannosaurus rex is present in the maxilla, with it exhibiting variability in depth and in the size and shape of the lacrimal and jugal processes. More recent, quantitative research on larger-scale (macro-evolutionary) issuesacross Theropoda indicates that cranial anatomy in this clade is quite variable, with major differ-ences seen in anteroposterior length and snout depth, and to a lesser extent, in orbit size and depth of the cheek region (Brusatte et al. 2012; Foth and Rauhut 2013a). These studies have shown that snout shape and length of the postorbital region ultimately position theropods into different regions of cranial morphospace. Although we have a relatively thor-ough understanding of alpha taxonomy, phylogenetics, and basic aspects of cranial shape disparity, there have been relatively few descriptions of ontogenetic changes in the
Fig. 1. Whole (B) and partial (A) skulls (rendered CT images) of Majungasauruscrenatissimus (Depéret, 1896) Lavocat, 1955 from the Maastrichtian (Late Cretaceous) Maevarano Formation, northwestern Madagascarin left lateral view. A. UA 9944. B. FMNH PR 2100. C. Illustration of landmark
positions used for articulated skull. Black circles, landmarks; white circles interconnected with solid lines, semilandmarks. D. Ontogenetic shape change
skull of theropod dinosaurs (but see Carr 1999; Carr and Williamson 2004; Rauhut and Fechner 2005; Bever and Norell 2009; Tsuihiji et al. 2011; Bhullar et al. 2012; Canale et al. 2015; Foth et al. 2016).
Previous morphometric work has focused on theropods such as Allosaurus and Tyrannosaurus (Chapman 1990), with only limited work specifically focused on ceratosau-rians (e.g., Carnotaurus and Ceratosaurus; Mazzetta et al. 1998). One study that did include information from abelisau-rids investigated the interspecific cranial shape variation in 35 species of non-avian theropods and basal birds (Foth and Rauhut 2013a). Skull shape in abelisaurids was found to dif-fer greatly from those of other large bodied predators, being characterized by an unusually deep and short skull (see also Brusatte et al. 2012; Foth et al. 2016). Building on this gen-eral context, this study focuses on characterizing changes in skull shape in a growth series in an exemplar abelisaurid. The specific aim of this morphometric analysis is to ex-amine ontogenetic changes in the skull of Majungasaurus crenatissimus, using both individual bones and whole/par-tial skulls, in order to understand the post-hatching devel-opment of the characteristic tall and wide abelisaurid skull morphotype.
Institutional abbreviations.—FMNH PR, Field Museum of Natural History, Chicago, IL, USA; UA, Université d’Anta-nanarivo, Madagascar.
Material and methods
The number of specimens currently assigned to Majunga-saurus crenatissimus is the largest for any of abelisaurids (Krause et al. 2007; O’Connor et al. 2011), consisting of at least eight partial skulls and skeletons. In this project we compared skulls that shared at least four bones that span the rostral, middle, and caudal regions of the cranium to characterize the skull as a coherent structure. Tables 1 and 2 provide a list of specimens used in the current study.
In order to interpret ontogenetic shape change in in-dividual cranial bones, we used a combination of 2D and 3D landmark-based geometric morphometric techniques (Fig. 2). For seven bones (premaxilla, maxilla, lacrimal, postorbital, jugal, dentary, and surangular), 2D landmarks and semilandmarks were used. For the quadrate, 3D land-marks and semilandland-marks were used to summarize its shape. Point landmarks and semilandmarks were assigned using either tpsDig v2.17 (2D; Rohlf 2013) or Landmark (3D; Wiley et al. 2005), with the coordinate data analyzed using the Geomorph package in R (Adams and Otárola-Castillo 2013). A list containing an anatomical description of the po-sition of each landmark is provided in Supplemental Table 1. In both approaches all landmarks are Type 2 landmarks (i.e., landmarks that exhibit evidence for geometric homology, such as points of maximal curvature or extremities) in the
A
B
C
E
D
2D3D
designate landmarks apply generalized procrustes analysis generate shape change visualizations
F
Fig. 2.Landmarks and semilandmarks designated using tpsDIG for 2D data (A) and landmark for 3D data (B). Landmark configurations aligned using
generalized procrustes analysis, removing the effects of size, orientation, and position (C, D). Ontogenetic shape change visualized by generating
terminology of Bookstein (1991). Following landmark digi-tization, identical analytical methods were used for both 2D and 3D data sets. Landmark configurations were subjected to a Generalized Procrustes Alignment (GPA), removing the effects of size, rotation, and position. We also calculated centroid size of each landmark configuration and we used centroid size to determine the smallest and largest speci-mens for each bone. In addition, the surface texture (e.g., the relative development of surface rugosity; Carr 1999; Canale et al. 2015) was also noted as another proxy of relative skele-tal maturity. For the seven 2D data sets, we illustrated shape change through ontogeny by generating deformation grids (geometric meshes) demonstrating how these smallest and largest shapes differ from the mean shape (Fig. 2E). These deformation grids were used to aid in interpretation of on-togenetic shape change. For the 3D data set, shape change through ontogeny was illustrated by “warping” a 3D volume of the smallest specimen to fit the landmark configuration of the largest specimen using thin-plate spline interpola-tion (Fig. 2F; Wiley et al. 2005). Although cranial material of Majungasaurus crenatissimus is remarkably well repre-sented, the available sample size is not high enough to facil-itate a statistical analysis of ontogenetic shape change. For this reason, we used these GMM geometric morphometric methods to provide a qualitative assessment of ontogenetic shape change rather than to conduct a quantitative analysis.
Results
Examined individually, each cranial bone shows ontogenetic shape change. The major change in premaxilla morphology is a decrease in the angle between the nasal process and the dorsal margin of the body of the premaxilla and a relative increase in length of the nasal process. This is most marked when comparing FMNH PR 3369 and FMNH PR 2278 (Fig. 3). Shape change in the maxilla was analyzed with land-marks and semilandland-marks placed around the perimeter of the maxillary body as incomplete preservation of the ascend-ing ramus makes designatascend-ing homologous landmarks in the vertical part of this bone impossible. The principal changes in maxilla morphology relate to an increase in height of the rostral part of the maxillary body and a decrease in the degree of sinuosity along the ventral margin. This is best
observed by comparing UA 9944 and FMNH PR 2278 (Fig. 4). From a qualitative point of view, the external rugosity (or texturing) on the lateral surface of the maxilla increases with size, as with the other dermal bones of the skull.
Some of the most notable ontogenetic changes in mor-phology were seen in the bones that surround the orbital and temporal regions of the skull. Although only two lacrimals were available for the analysis, it is apparent that there are major changes in both the overall geometry of the bone and its constituent subparts that influence adjacent craniofacial features (e.g., size of the orbit) from small to large forms
Table 1. List of isolated elements of Majungasauruscrenatissimus used in this study.
Accession numbers of specimens Element Number of specimens
Number of landmarks
Number of semilandmarks FMNH PR 2278, FMNH PR 3369, UA 8716, UA 8717, UA 9944 premaxilla 5 7 8 FMNH PR 2100, FMNH PR 2278, FMNH PR 3369, UA 9944 maxilla 4 7 3 FMNH PR 2100, UA 9944 lacrimal 2 11 16 FMNH PR 2100, FMNH PR 3369, UA 9944 postorbital 3 7 10 FMNH PR 2100, FMNH PR 3399, UA 9944 jugal 3 6 2 FMNH PR 2100, FMNH PR 2278, FMNH PR 3369, UA 9944, UA 10000 quadrate 5 9 16 FMNH PR 2100, FMNH PR 3369, UA 9944 dentary 3 12 24 FMNH PR 2100, FMNH PR 3369, UA 9944 surangular 3 5 5
(Fig. 5). Specifically, there is a relative decrease in the dor-soventral height of the whole bone, a general increase in size of the lacrimal body, and a decrease in the circum-ference of the orbital margin formed by the lacrimal. The decrease results from both deposition of bone around the orbital margin of the lacrimal and an increase in relative size of the sub-orbital process. Also, the morphology of the ros-tral ramus changes substantially, where it extends rosros-trally in the small form, but is significantly curved rostroventrally (equally rostral and ventral) in the large form (Fig. 5). Given the limited sample size, the incorporation of additional lac-rimals is essential to distinguish whether this latter feature is indeed size related, or rather, if it pertains to intraspecific variability.
Three postorbitals were compared in this analysis, where the dorsal margin is relatively rostrocaudally short in the large mature bones. There is also narrowing of the orbital margin (i.e., the part of the postorbital that is clos-est to the lateral aperture of the orbit; Fig. 6), similar to that observed above for the lacrimal. Three jugals were compared in the study, where there is a relative increase in dorsoventral height of the lacrimal process and a gen-eralized relative increase in the rostrocaudal length of the bone expressed in the rostral part of the bone, the base of the suborbital process, and the caudal part of the bone (i.e., at the quadratojugal process). These changes coincide with an increase in the dorsoventral height of the articulation between the quadratojugal and jugal (Fig. 7). Notable dif-ferences in the quadrate shape across the growth series in-clude a relative decrease in the caudally-directed concavity and in increase in height of the dorsal half of the quadrate shaft (Fig. 8; also see videos at SOM 3 and 4, available at http://app.pan.pl/SOM/app61-Ratsimbaholison_etal_SOM. pdf). Although the quadrate was examined in 3D, the major differences through the growth series are best appreciated in lateral view. Mandibular bones variably exhibit ontoge-netic shape change as well. A series of three dentaries show major changes including a relative increase in overall height and a change from angular to rounded rostroventral corner
convexity (Fig. 9). Three surangulars were included in the analysis, with little noticeable differences apparent over the size range examined (Fig. 10).
Three partial associated or articulated skulls of Majunga-sauruscrenatissimus, ranging in estimated length from 42 cm to 53 cm (SOM 2), were included in a multi-element analysis. The use of these specimens served to identify any skull
char-Fig. 4. Representative maxillae (rendered CT images) of Majungasauruscrenatissimus (Depéret, 1896) Lavocat, 1955 from the Maastrichtian (Upper Cretaceous) Maevarano Formation, northwestern Madagascar in right lateral view. A. UA 9944. B. FMNH PR. 3369. C. FMNH PR 2278. D. Illustration
of landmark positions used for maxillae. Black circles, landmarks. E. Ontogenetic shape change visualized by deformation grids relative to average;
out-line of smallest (E1) and largest (E2) specimens from average.
Fig. 5. Representative lacrimals (rendered CT images) of Majungasaurus crenatissimus (Depéret, 1896) Lavocat, 1955 from the Maastrichtian (Upper Cretaceous) Maevarano Formation, northwestern Madagascar in left lateral view. A. UA 9944. B. FMNH PR 2100. C. Illustration of
land-mark positions used for lacrimals. Black circles, landland-marks; white circles interconnected with solid lines, semilandmarks. D. Ontogenetic shape
acteristics related to changes in the nature of articulations among elements over the growth series. Despite the fact that M. crenatissimus is known from many specimens of diverse ontogenetic (size) classesand represents a good candidate for ontogenetic research, many of the partial skulls provide lim-ited information for the current study. Specifically, nonover-lapping preservation of bones (Fig. 1A–C) renders the dataset useful for characterizing selected regions (e.g., postorbital region), whereas it limits potential information from other re-gions (e.g., rostrodorsal narial region). In sum, 17 landmarks and 16 semilandmarks were compared for these three skulls in a 2D, lateral view perspective (Fig. 1).
Examination of the skull shape deformation grids reveals several growth changes in the skull. First, there is a relative
increase in dorsoventral height of the lacrimal process of the jugal and rostrocaudal length of the rostral part of the jugal. These changes coincide with an increase in the dorsoventral height of the articulation between the quadratojugal and ju-gal. The orientation of the jugal is rotated in larger individ-uals such that the contact between the jugal and maxilla is positioned relatively more dorsal than the jugal-quadratoju-gal contact. Second, the orbit becomes smaller relative to the size of the skull. For example, the ventral portion of the orbit becomes taller and rostrocaudally shorter. This corresponds to a shortening of the jugal process of the quadratojugal. The caudal margin of the dorsal region of the orbit (i.e., the orbit proper) decreases in diameter. Finally, the temporal region of the skull increases in height due to the relative
Fig. 6. Representative postorbitals (rendered CT images) of Majungasauruscrenatissimus (Depéret, 1896) Lavocat, 1955 from the Maastrichtian (Upper Cretaceous) Maevarano Formation, northwestern Madagascar in right lateral view. A. UA 9944. B. FMNH PR 3369. C. FMNH PR 2100. D. Illustration
of landmark positions used for postorbitals. Black circles, landmarks; white circles interconnected with solid lines, semilandmarks. E. Ontogenetic shape
change visualized by deformation grids relative to average; outline of smallest (E1) and largest (E2) specimens from average.
Fig. 7. Representative jugals (rendered CT images) of Majungasauruscrenatissimus (Depéret, 1896) Lavocat, 1955 from the Maastrichtian (Upper Cretaceous) Maevarano Formation, northwestern Madagascar in right lateral view. A. UA 9944. B. FMNH PR 3369. C. FMNH PR 2100. D. Illustration
of landmark positions used for jugals. Black circles, landmarks. E. Ontogenetic shape change visualized by deformation grids relative to average; outline
increase in height between the squamosal process of postor-bital and quadrate process of quadratojugal, which changes the inclination of the jugal (Fig. 1).
Discussion
This study has resulted in a number of observations related to craniomandibular skeletal ontogeny in Majungasaurus crenatissimus. These changes may be consistent with pat-terns in abelisaurids in general given the shared possession of tall, short skulls in the clade. The fossil record of M. crenatissimus is notable (n = 8 partial/whole skulls) among Abelisauridae, but is still too limited to allow for rigorous statistical evaluation of shape change (e.g., significance of allometric shape change). Nonetheless, our results provide important observations for refining primary hypotheses re-garding skull shape change through ontogeny in the group. Ontogenetic shape change in individual elements.—Dif fe-rential growth in portions of numerous skull bones (e.g., max-illa, quadrate) contribute to the tall skull of larger specimens of Majungasaurus crenatissimus. Throughout ontogeny, these elements undergo dorsoventral expansion, as seen in the comparison plots of individual elements (e.g., Figs. 3–9).
Taken together, it is apparent that individual skull elements or even component parts of them contribute to the overall adult morphotype seen in Majungasaurus (i.e., high skull).
Ontogenetic shape change of the skull.—Analysis of the articulated skull is also consistent with ontogenetic dorso-ventral expansion. Importantly, only certain regions (e.g., the rostral-most maxilla) of bones making up the rostrum increase in dorsoventral height, whereas the caudal por-tion of the maxilla is not expanded to the same degree. In contrast, the entire quadrate contributes to increase in dorsoventral height of the skull. This is best exemplified in the increase in height between the squamosal process of the postorbital and the quadrate process of the quadratojugal (Fig. 10). In addition, the orientation of the long axis of the body of the jugal shifts from being relatively horizontal to having a caudoventral-to-rostrodorsal orientation in larger specimens. Such changes in orientation through ontogeny contribute to the characteristic tall skull of Majungasaurus and abelisaurids more generally.
Other observations related to ontogenetic changes in
Majun ga saurus crenatissimus.—Both individual element
(e.g., postorbital) and whole skull analyses show changes to the orbit. For example, orbital circumference decreases due
Fig. 8. Representative right quadrates (rendered CT images) of Majungasauruscrenatissimus (Depéret, 1896) Lavocat, 1955 from the Maastrichtian (Upper Cretaceous) Maevarano Formation, northwestern Madagascar in left lateral view. A. UA 10000. B. UA 9944. C. FMNH PR 3369. D–F. Landmark
positions in anterior (D), left lateral (E), and posterior (F) views. G, H. Warped meshes, rostral (G) and lateral (H) views, showing idealized
to closing of the arc formed along the orbital margin on both the lacrimal and postorbital (Figs. 5, 6). A similar ontoge-netic change in orbit shape is seen in other theropods (e.g., Henderson 2002; Foth and Rauhut 2013a; see below). There also appears to be increased connectivity (e.g., sutural rigid-ity) between bones and changes in the general surface tex-ture of the skull. It is apparent that sutex-tures between adjacent bones become increasingly interlocked during growth. This is best illustrated by the sutural connection between the quadratojugal and jugal, and between the jugal and maxilla (Fig. 1). There is an increase the rugose sculpturing on the external surfaces of many of the skull elements in M. crena-tissimus. Rugose external bone texture has been described as one of the hallmark abelisaurid features (e.g., Sampson and Witmer 2007; Hieronymus 2009; also, see Canale et al. 2015 for additional discussion of this feature in other non-avian theropods). The increasing sculpturing/rugosity of the external surfaced is so pronounced in the larger individuals that it obscures sutural boundaries (e.g., between the postor-bital and lacrimal; Fig. 1).
Intraspecific variation.—Although the current study sought to examine shape changes in individual elements and whole/ partial skulls of Majungasaurus crenatissimus as a repre-sentative abelisaurid, results from this work also point out significant intraspecific variability that is either completely independent of size-related changes or not directly linked with changes in growth/size. For example, a decrease in the degree of sinuosity along the ventral margin of the maxilla is apparent through the series (Fig. 4). Moreover, even a simple qualitative assessment of maxilla morphology indicates dif-ferences related to the lateral exposure of the antorbital fenes-tra. Specifically, a comparison of two, similar-sized maxillae reveal one specimen (UA 9944) in which the lateral antorbital fossa (sensu Hendrickx and Mateus 2014) is well exposed, with the other specimen (FMNH PR 3369) exhibiting a virtu-ally nonexistent lateral exposure of the antorbital fossa along the jugal ramus (Fig. 4B, C). It is important to note that such
differences existing within a single taxon could have signif-icant implications for assessing the taxonomic uniqueness (i.e., putative autapomorphies) of isolated discoveries (e.g., Russell 1996; Lamanna et al. 2002) or remains that preserve rather limited anatomical information.
Biomechanical implications of ontogenetic skull change.— The disproportionate dorsoventral increase in height of the adductor region of the skull implies that adductor muscle length would have had a similar allometric relationships through ontogeny. It is unclear how this might affect bite force production, as there is little constraint on general mus-cle architecture (e.g., pennate or not) or specific architec-tural parameters (e.g., degree of pennation) for specific jaw adductors (Holliday 2009; Sakamoto 2010). Importantly, work on other theropods (e.g., Foth and Rauhut 2013a) and extant crocodylians (e.g., Pierce et al. 2008; Foth et al. 2013) has also found shape change differences between the rostal and caudal (i.e., posterior) ends of the skull, suggesting the former relates more to dietary preference (e.g., prey type) and the latter to general allometric considerations related to maintenance of function at larger sizes (e.g., the necessity of producing higher bite forces) and feeding behavior more generally. As such, the observed increase in height of the adductor region in M. crena tissimus is consistent in this context, particularly when considering its typical “carniv-orous” theropod morphology in dentigerous elements (Foth and Rauhut 2013a). The ontogeny of bite-force generation is positively allometric (e.g., Erickson et al. 2003; also see Erickson et al. 2012 for a more general discussion of the allometry of bite force production in a comparative con-text). It should also be appreciated, however, that general increases in fiber length (inferred on the basis of positive ontogenetic allometry of the adductor chamber) contribute to both a wider gape and an increased range over which bite forces may be applied to substrates (Herring and Herring 1974, Lautenschlager 2015). Thus, the significance of the observed ontogenetic changes in adductor chamber mor-Table 2. List of Majungasauruscrenatissimus skull specimens used in this study (whole skulls). Locality abbreviation: MAD YY-XX, Madagas-car Paleontology Project (formerly Mahajanga Basin Project) locality identifier, with the year of discovery of that locality (YY) and the locality number for that year (XX).
Accession number Locality Skull elements preserved
FMNH PR 2100 MAD 96-01 nearly complete, exquisitely preserved, disarticulated skull (see Sampson and Witmer 2007 for complete list of elements)
FMNH PR 2278 MAD 99-26 associated cranial material (both premaxillae, both maxillae, left jugal, left quadratojugal, left ectoptery-goid, left quadrate, left surangular, left angular, left prearticular and left articular)
UA 9944 MAD 05-42 left dentary and splenial, both postorbitals, left premaxilla, both ectopterygoids, right maxilla, both jugals, both lacrimals, both quadrates, right splenial, right squamosal, right quadratojugal, both surangulars, both angulars
FMNH PR 3369 MAD 05-42 right maxilla, right postorbital, right surangular, right quadrate (note: additional elements are preserved, but not yet prepared for this skull)
UA 9944 MAD 05-42 left: dentary, premaxilla; both: postorbitals, jugals, splenials, ectopterygoids, lacrimals, quadrates, suran-gulars, angulars; right: maxilla, squamosal, quadratojugal
FMNH PR 3369 MAD 05-42 right maxilla, right postorbital, right surangular, right quadrate (note: additional elements are preserved, but not yet prepared for this skull)
phology for feeding mechanics in abelisaurids remains to be clarified, particularly given that the feeding mechanics in M. crena tissimus (and other abelisaurids) have only been superficially addressed (e.g., jaw adduction vs. jaw adduc-tion combined with pulling; O’Connor 2007; Sampson and Witmer 2007; Méndez 2014).
Comparative ontogeny of the non-avian theropod skull.— The ontogenetic changes in skull shape seen in M. crena-tissimus differ from the patterns typically seen among non-avian theropod dinosaurs. Most non-eumaniraptoran theropods (e.g., Coelophysis, Compsognathidae) increase the length of the face and decrease the height of the lower temporal fenestra through ontogeny, resulting in a more slender skull in adults than in juveniles (Bhullar et al. 2012). The opposite is seen in M. crena tissimus, which has a taller skull and temporal region in adults than juveniles. However, this trend compares favorably to patterns in so-called “giant theropods” of various clades, including ceratosaurs, allo-sauroids, and tyrannosauroids (Bhullar et al. 2012). The giant taxa exhibit a novel developmental trajectory that is
similar to the “typical” theropod condition (i.e., rostrocau-dal elongation), but this changes to an increase of the dorso-ventral dimension of the skull (Bhullar et al. 2012), resulting in a tall skull. This ontogenetic pattern is hypothesized to have evolved convergently in all large-bodied theropods (Bhullar et al. 2012) and is likely to be an example of per-amorphic heterochrony (Canale et al. 2015). As the skull of Majungasaurus also increases in height through ontogeny, it is possible that it shares the developmental trajectory of other large-bodied theropods. Additional perinatal or very small juvenile specimens are needed to determine whether Majungasaurus transitions through an initial phase of elon-gation before increasing in height, similar to the pattern observed in Tyrannosaurus and other large-sized theropods.
Conclusions
The ontogenetic skull changes of Majungasaurus crenatissi-mus include (i) increase in skull height, (ii) increased sutural
Fig. 10. Representative surangulars (rendered CT images) of Majungasauruscrenatissimus (Depéret, 1896) Lavocat, 1955 from the Maastrichtian (Upper Cretaceous) Maevarano Formation, northwestern Madagascar in left lateral view. A. FMNH PR 3369. B. FMNH PR 2100. C. Illustration of
land-mark positions used for surangulars, UA 9944 (not to scale). Black circles, landland-marks; white circles interconnected with solid lines, semilandland-marks.
D. Ontogenetic shape change visualized by deformation grids relative to average; outline of smallest (D1) and largest (D2) specimens from average.
Fig. 9. Representative dentaries (rendered CT images) of Majungasauruscrenatissimus (Depéret, 1896) Lavocat, 1955 from the Maastrichtian (Upper Cretaceous) Maevarano Formation, northwestern Madagascar in left lateral view. A. MAD 10440. B. FMNH PR 2100. C. Illustration of landmark
posi-tions used for dentaries. Black circles, landmarks; white circles interconnected with solid lines, semilandmarks. D. Ontogenetic shape change visualized
interlocking between cranial elements, and (iii) increased surface texturing on certain elements (e.g., maxilla) as size increases. The overall shape differences in the growth series are achieved through shape changes in individual elements including the quadrate, postorbital, lacrimal and jugal, in addition to differential growth in some sub-regions of in-dividual elements (e.g., the rostral part of the maxilla). This effort characterizes craniomandibular ontogeny in an exem-plar abelisaurid, one necessary step for understanding the extensive radiation of the group throughout Gondwanan and better placing it in an ecological setting.
Acknowledgements
A very special thanks to Joseph Groenke (Stony Brook University, USA) for the preparation, molding, casting, and CT-scanning of all pre-viously-unpublished Majungasaurus crena tissimus specimens used in this study. We also thank David Krause (Stony Brook University), Joseph Sertich (Denver Museum of Science and Nature, USA), Eric Lund and Waymon Holloway (both Ohio University, Athens, USA), and other members of the Mahajanga Basin Project for advice and logistical support during the development and execution of this proj-ect. Haingoson Andriamialison and Armand Rasoamiaramanana (Department of Paleontology and Biological Anthropology, University of Antananarivo, Madagascar) are thanked for their support. Susan Williams (Ohio University), Casey Holliday (University of Missouri, Columbia, USA), and Lawrence Witmer (Ohio University) provided useful discussions. Christian Foth (University of Fribourg, Switzer-land) and Thomas Carr (Carthage College, Kenosha, Wisconin, USA) are thanked for providing comments on an earlier version of this manuscript. This work was supported by the National Science Foundation (EAR-0446488, EAR-0617561, and EAR-1123642), the Ohio University Office of Research and Sponsored Programs, the Ohio University Heritage College of Osteopathic Medicine, and SVP SEDN-Program for Scientists from Economically Developing Nations.
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